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Genetic Diversity of Barley Foliar Fungal Pathogens

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agronomy Review Genetic Diversity of Barley Foliar Fungal Pathogens Arzu Çelik O˘guz* and Aziz Karakaya Department of Plant Protection, Faculty of Agriculture, Ankara University, Dı¸skapı,Ankara 06110, Turkey; [email protected] * Correspondence: [email protected] Abstract: Powdery mildew, net blotch, scald, spot blotch, barley stripe, and leaf rust are important foliar fungal pathogens of barley. Fungal leaf pathogens negatively affect the yield and quality in barley plant. Virulence changes, which can occur in various ways, may render resistant plants to susceptible ones. Factors such as mutation, population size and random genetic drift, gene and genotype flow, reproduction and mating systems, selection imposed by major gene resistance, and quantitative resistance can affect the genetic diversity of the pathogenic fungi. The use of fungicide or disease-resistant barley genotypes is an effective method of disease control. However, the evolutionary potential of pathogens poses a risk to overcome resistance genes in the plant and to neutralize fungicide applications. Factors affecting the genetic diversity of the pathogen fungus may lead to the emergence of more virulent new pathotypes in the population. Understanding the factors affecting pathogen evolution, monitoring pathogen biology, and genetic diversity will help to develop effective control strategies. Keywords: barley; Hordeum vulgare; Blumeria graminis; Pyrenophora teres; Rhynchosporium commune; Cochliobolus sativus; Pyrenophora graminea; Puccinia hordei; genetic diversity Citation: Çelik O˘guz,A.; Karakaya, A. Genetic Diversity of Barley Foliar Fungal Pathogens. Agronomy 2021, 11, 1. Introduction 434. https://doi.org/10.3390/ Barley (Hordeum vulgare L.) is one of the most important cereal crops that has been agronomy11030434 grown for thousands of years since prehistoric times, and is used in animal feed, malt products, and the food industry. Globally, it ranks fourth in grain production with approxi- Academic Editors: Giuseppe De mately 150 million tons of production after wheat, rice, and maize [1]. Mastro and Caterina Morcia Barley leaf diseases cause significant decreases in yield in all areas where barley is cultivated, and at the same time, reduces the quality. The use of fungicides or disease- Received: 31 December 2020 resistant barley genotypes is effective in disease control, but the evolutionary potential Accepted: 22 February 2021 of pathogens poses a risk of overcoming resistance genes in the plant and neutralizing Published: 27 February 2021 fungicide applications [2–4]. Information about the evolutionary potential of pathogens is useful in developing control strategies [5–7]. Publisher’s Note: MDPI stays neutral The genetic makeup of a pathogen population is determined by the evolutionary with regard to jurisdictional claims in history of that population. It is assumed that genetic makeup information also gives published maps and institutional affil- an idea of the evolutionary potential of pathogen populations in the future. Genetic iations. structure refers to the distribution and amount of genetic diversity among and within populations. Genotype diversity and gene diversity are components of genetic makeup. Gene diversity refers to the number and frequencies of alleles in a population at individual loci, while genotype diversity refers to the genetically distinct individuals or the number Copyright: © 2021 by the authors. and frequencies of multilocus genotypes in a population [7]. Licensee MDPI, Basel, Switzerland. Changes in pathogen populations have been witnessed many times over the years [8]. This article is an open access article The most devastating changes in history have been reported in pathogenic populations distributed under the terms and capable of breaking major resistance genes [9–11]. Most of these cases have resulted from conditions of the Creative Commons the spread of a host plant carrying a single major resistance gene over a wide geographic Attribution (CC BY) license (https:// area and occurred as a result of the pathogen population developing a means to overcome creativecommons.org/licenses/by/ 4.0/). this resistance gene [7]. Agronomy 2021, 11, 434. https://doi.org/10.3390/agronomy11030434 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, 434 2 of 27 To understand the process by which the effectiveness of the resistance gene is broken down, the processes governing pathogen evolution must be understood. The genetic makeup and evolution of populations is a result of the interaction between the five forces: mutation, reproduction and mating system, gene and genotype flow, population size and random drift, major gene resistance, and selection imposed by major gene resistance and quantitative resistance. Mutation is one of the sources of genetic variation. As a result of mutations, changes in the DNA sequence of individual genes occur and these generate new alleles in populations. New virulent strains of plant pathogens can be formed through the mutations and these could break the major gene resistances. Population size affects the likelihood that mutants will be present. More mutants are observed in large populations compared to small populations and these can affect the diversity of genes in a population through random genetic drift. Disease management programs or climatic extremes that keep pathogen population size small, limit gene diversity and help to control the disease [4,6,7]. Gene flow is a process in which certain genotypes or genes are exchanged among populations. Greater genetic diversity is possible with pathogens that display a high degree of genotype/gene flow. Anthropogenic activities can affect the size of the genetic neighborhood. Humans have transported many different pathogens well beyond distri- bution borders through agriculture and intercontinental travel and trade [7]. Distribution of gene diversity among and within populations is affected by reproduction and mating systems. Reproduction can be mixed, asexual, or sexual. Pathogens that undergo regular recombination may pose greater risks [7,12]. Female fertility is much more important than the relative numbers of strains of differ- ent mating types in determining the given effective population size obtained from Gibberella species. Even when mating-type ratios differ significantly from 1:1, sexual reproduction can still occur regularly. In field populations, polymorphism occurs when the female is sterile or hermaphrodite, and only those female sterile mutants that function as males during sexual reproduction can make up the majority of the population. When a high frequency of female sterile strains is observed in field populations, this indicates that vegetative propagation is an important component of the natural history of the fungus. This theory suggests that there may be significant differences in female fertility between populations of the same species, and within the same species, the frequency of hermaphrodites in local populations may vary significantly. Additionally, if there are significant environmen- tal differences that support sexual reproduction or vegetative reproduction in different places, these differences may become apparent, and the number of loci where female sterile mutations can occur might be large and mutations can be found in more than one locus rather than a single locus. These hypotheses will provide an insight into the evolution of asexual fungus species and how fungi maintain mixed modes of vegetative and sexual reproduction [13]. Selection cause changes in the mutant allele frequencies. When a major resistance gene is widely distributed over a wide geographic area, directional selection occurs [4,14]. Quantitative resistance is another option for obtaining resistant varieties. This is also called partial resistance or minor-gene resistance. Quantitative resistance does not exhibit the boom-and-bust cycle, which is characteristic of major resistance genes. Both minor and major gene resistances can be sensitive to environmental conditions [6,7]. Classification of genetic variation in fungi based on morphological characteristics affected by environmental conditions is very difficult. For characterization of genetic varia- tion and phylogenetic relationships in fungal plant pathogenic populations, techniques such as isozyme and ribosomal DNA analyses, restriction fragment length polymorphism (RFLP), restriction of PCR-amplified internal transcribed spacers of the rDNA (ITS-RFLP), random amplified polymorphic DNA (RAPD) markers, amplified fragment length poly- morphism (AFLP), universal rice primer-polymerase chain reaction (URP-PCR), sequence- specific amplified polymorphism (S-SAP), inter-retrotransposon amplified polymorphism Agronomy 2021, 11, 434 3 of 27 (IRAP), inter simple sequence repeat (ISSR) markers, single nucleotide polymorphism (SNP) markers in housekeeping genes and simple sequence repeat (SSR) markers are used. The result of understanding genetic variation in fungal pathogens is to understand the risk of pathogen evolution and planning resistance breeding strategies. The genetic variation of common barley fungal leaf pathogens is discussed in this review. 1.1. Blumeria graminis (DC.) E. O. Speer f. sp. hordei emend. É. J. Marchal (anamorph: Oidium monilioides Link) Powdery mildew disease caused by the ascomycetous fungus Blumeria graminis (DC) Speer (Syn. Erysiphe graminis DC) is one of the most destructive pathogens of barley crops in many barley production areas of the world [15,16]. In connection
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    INDUSTRY BIOSECURITY PLAN FOR THE GRAINS INDUSTRY Threat Specific Contingency Plan Net form of net blotch (exotic pathotypes) Pyrenophora teres f. sp. teres Prepared by Trevor Bretag and Plant Health Australia May 2009 PLANT HEALTH AUSTRALIA | Contingency Plan – Net form of net blotch (Pyrenophora teres f. sp. teres) Disclaimer The scientific and technical content of this document is current to the date published and all efforts were made to obtain relevant and published information on the pest. New information will be included as it becomes available, or when the document is reviewed. The material contained in this publication is produced for general information only. It is not intended as professional advice on any particular matter. No person should act or fail to act on the basis of any material contained in this publication without first obtaining specific, independent professional advice. Plant Health Australia and all persons acting for Plant Health Australia in preparing this publication, expressly disclaim all and any liability to any persons in respect of anything done by any such person in reliance, whether in whole or in part, on this publication. The views expressed in this publication are not necessarily those of Plant Health Australia. Further information For further information regarding this contingency plan, contact Plant Health Australia through the details below. Address: Suite 5, FECCA House 4 Phipps Close DEAKIN ACT 2600 Phone: +61 2 6260 4322 Fax: +61 2 6260 4321 Email: [email protected] Website: www.planthealthaustralia.com.au | PAGE 2 PLANT HEALTH AUSTRALIA | Contingency Plan – Net form of net blotch (Pyrenophora teres f.
  • Supplementary Table S1 18Jan 2021

    Supplementary Table S1 18Jan 2021

    Supplementary Table S1. Accurate scientific names of plant pathogenic fungi and secondary barcodes. Below is a list of the most important plant pathogenic fungi including Oomycetes with their accurate scientific names and synonyms. These scientific names include the results of the change to one scientific name for fungi. For additional information including plant hosts and localities worldwide as well as references consult the USDA-ARS U.S. National Fungus Collections (http://nt.ars- grin.gov/fungaldatabases/). Secondary barcodes, where available, are listed in superscript between round parentheses after generic names. The secondary barcodes listed here do not represent all known available loci for a given genus. Always consult recent literature for which primers and loci are required to resolve your species of interest. Also keep in mind that not all barcodes are available for all species of a genus and that not all species/genera listed below are known from sequence data. GENERA AND SPECIES NAME AND SYNONYMYS DISEASE SECONDARY BARCODES1 Kingdom Fungi Ascomycota Dothideomycetes Asterinales Asterinaceae Thyrinula(CHS-1, TEF1, TUB2) Thyrinula eucalypti (Cooke & Massee) H.J. Swart 1988 Target spot or corky spot of Eucalyptus Leptostromella eucalypti Cooke & Massee 1891 Thyrinula eucalyptina Petr. & Syd. 1924 Target spot or corky spot of Eucalyptus Lembosiopsis eucalyptina Petr. & Syd. 1924 Aulographum eucalypti Cooke & Massee 1889 Aulographina eucalypti (Cooke & Massee) Arx & E. Müll. 1960 Lembosiopsis australiensis Hansf. 1954 Botryosphaeriales Botryosphaeriaceae Botryosphaeria(TEF1, TUB2) Botryosphaeria dothidea (Moug.) Ces. & De Not. 1863 Canker, stem blight, dieback, fruit rot on Fusicoccum Sphaeria dothidea Moug. 1823 diverse hosts Fusicoccum aesculi Corda 1829 Phyllosticta divergens Sacc. 1891 Sphaeria coronillae Desm.
  • Isolation and Characterization of the Mating-Type Locus of the Barley

    Isolation and Characterization of the Mating-Type Locus of the Barley

    855 Isolation and characterization of the mating-type locus of the barley pathogen Pyrenophora teres and frequencies of mating-type idiomorphs within and among fungal populations collected from barley landraces Domenico Rau, Frank J. Maier, Roberto Papa, Anthony H.D. Brown, Virgilio Balmas, Eva Saba, Wilhelm Schaefer, and Giovanna Attene Abstract: Pyrenophora teres f. sp. teres mating-type genes (MAT-1: 1190 bp; MAT-2: 1055 bp) have been identified. Their predicted proteins, measuring 379 and 333 amino acids, respectively, are similar to those of other Pleosporales, such as Pleospora sp., Cochliobolus sp., Alternaria alternata, Leptosphaeria maculans, and Phaeosphaeria nodorum. The structure of the MAT locus is discussed in comparison with those of other fungi. A mating-type PCR assay has also been developed; with this assay we have analyzed 150 isolates that were collected from 6 Sardinian barley land- race populations. Of these, 68 were P. t e re s f. sp. teres (net form; NF) and 82 were P. t e re s f. sp. maculata (spot form; SF). Within each mating type, the NF and SF amplification products were of the same length and were highly similar in sequence. The 2 mating types were present in both the NF and the SF populations at the field level, indicating that they have all maintained the potential for sexual reproduction. Despite the 2 forms being sympatric in 5 fields, no in- termediate isolates were detected with amplified fragment length polymorphism (AFLP) analysis. These results suggest that the 2 forms are genetically isolated under the field conditions. In all of the samples of P.
  • The Response of Some Spring Barley Cultivars Grown in Finland to Air-Borne Secondary Infection by Bipolaris Sorokiniana of Infe

    The Response of Some Spring Barley Cultivars Grown in Finland to Air-Borne Secondary Infection by Bipolaris Sorokiniana of Infe

    JOURNAL OF AGRICULTURAL SCIENCE IN FINLAND Maataloustieteellinen Aikakauskirja Vol. 57: 97—105, 1985 The response of some spring barley cultivars grown in Finland to air-borne secondary infection by Bipolaris sorokiniana AARNE KURPPA Department of Plant Pathology, University of Helsinki * SF-00710 HELSINKI 71, Finland Abstract. Air-borne secondary inoculum of Bipolaris sorokiniana caused severe foliar dis- eases and yield losses in all 12 spring barley cultivars tested in greenhouses or in the field. For secondary infection to occur a high relative humidity was necessary. Yield losses due to foliar diseases reached a maximum of 43.4 % in greenhouse experiments and 27.8 % in the field. The mean losses were 20.3 % and 12.3 %, respectively. Early infection at the time of heading or shortly after it resulted in higher yield losses than did later infection, although the symptom expression was opposite. Spore inoculation or natural secondary infection by the spores from a diseased crop after heading always resulted in a high infection incidence in the grain. Infec- tion incidence as well as fungal invasion of the internal cell leyers of the grains varied signifi- cantly among barley cultivars. The most susceptible of those tested were cvs. Teemu, Paavo and Pomo, while the most resistant were Ingrid, Otra and Pirkka. Introduction increasingly common in barley in the cool climate in North-Western Europe (Jorgen- sorokiniana (Sacc. in Sorok.) Bipolaris sen 1974, Hewett 1975, Mäkelä 1975, Shoem. (syn. Helminlhosporium sativum Kurppa 1984). & Cochlio- Pamm., King Bakke), perfect state Conidia of the fungus are the main sources sativus & Kurib.) has a world-wide bolus (Ito of infection, and are able to survive at least as a major pathogen of cereals distribution two years in soil (Ledingham 1970).
  • Resistance in Spring Wheat to the Various Diseases Caused By

    Resistance in Spring Wheat to the Various Diseases Caused By

    Resistance in spring wheat to the various diseases caused by Cochliobolus sativus by Aftabuddin Ahmed A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Plant Pathology Montana State University © Copyright by Aftabuddin Ahmed (1989) Abstract: Sixteen spring wheat cultivate were tested for their resistance to the various diseases caused by Cochliobolus sativus (Ito and Kurib.) Drechsl. ex Dastur. Five Montana isolates and four Bangladesh isolates of the fungus were used in whole plant inoculations in the Plant Growth Center and in laboratory tests using detached leaves. Sources of resistance were detected and identified for different phases of the disease. Ten cultivars were resistant to root rot, eight cultivars were resistant to foliar spot blotch, and six cultivars were resistant to head blight or black point. A number of cultivars showed differential reaction to various phases of the disease, e.g., were resistant to root rot but were susceptible to foliar spot blotch. Six cultivars, namely Marberg, GP248, GP253, GP254 and GP255, were resistant to all phases of the disease. The isolates tested differed significantly in pathogenicity, but considerable shifting in ranking occurred between experiments. Isolates obtained from roots were able to attack foliage/heads and vice versa. The isolates from Bangladesh did not have a higher temperature requirement than the USA isolates. Some cultivars were resistant to all isolates from both Bangladesh and the USA. The maximum disease development for root rot, foliar and head blight/black point phases occurred at 30°C with a 72 hour exposure to moist conditions. The disease reactions on detached leaves were not consistent with those on intact leaves.